Gastrin-releasing peptide receptor signaling in cancer

Cancer Therapy

Volumn 7, Issue ISSUE A, 2009, Pages 332-346

  Flores, Debora Gazzana ^a   Lenz, Guido ^a   Roesler, Rafael ^a,b   Schhwartsmann, Gilberto ^a,b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b National Institute for Translational Medicine   (Brazil)

Author keywords

Cancer; Cell signaling; Gastrin releasing peptide; Gastrin releasing peptide receptor

Indexed keywords

ANTINEOPLASTIC AGENT; BOMBESIN; BOMBESIN[6-13][6 DEXTRO PENTAFLUOROPHENYLALANINE 11 DEXTRO ALANINE] METHYL ESTER; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOOXYGENASE 2; EPIDERMAL GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 2; FORSKOLIN; GASTRIN RELEASING PEPTIDE RECEPTOR; GASTRIN RELEASING PEPTIDE RECEPTOR ANTAGONIST; GUANOSINE TRIPHOSPHATASE; PAXILLIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE D; PROTEIN TYROSINE KINASE; RAP1 PROTEIN; RHO FACTOR; UNCLASSIFIED DRUG;

CANCER CELL; CELL PROLIFERATION; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE ACTIVATION; GENE FUNCTION; GENE LOCATION; GENE OVEREXPRESSION; GENE SEQUENCE; GENE TARGETING; HUMAN; NONHUMAN; PHARMACOLOGICAL BLOCKING; REVIEW; SIGNAL TRANSDUCTION; TRANSACTIVATION; TUMOR GROWTH;

EID: 69949157370     PISSN: 15439135     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (147)

1. Ally RA, Ives KL, Traube E, Eltounsi I, Chen PW, Cahill PJ, Battey JF, Hellmich MR, Kroog GS (2003) Agonist- and protein kinase C-induced phosphorylation have similar functional consequences for gastrin-releasing peptide receptor signaling via Gq. Mol Pharmacol 64, 890-904.
2. Anastasi A, Erspamer V, Bucci M (1971) Isolation and structure of bombesin and alytesin, 2 analogous active peptides from the skin of the European amphibians Bombina and Alytes. Experientia 27, 166-7.
3. Aprikian AG, Han K, Chevalier S, Bazinet M, Viallet J (1996) Bombesin specifically induces intracellular calcium mobilization via gastrin-releasing peptide receptors in human prostate cancer cells. J Mol Endocrinol 16, 297-306.
4. Avis I, Jett M, Kasprzyk PG, Cuttitta F, Treston AM, Maneckjee R, Mulshine JL (1993) Effect of gastrin-releasing peptide on the pancreatic tumor cell line (Capan). Mol Carcinog 8, 214-20.
5. Bajo AM, Schally AV, Groot K, Szepeshazi K (2004) Bombesin antagonists inhibit proangiogenic factors in human experimental breast cancers. Br J Cancer 90, 245-52.
6. Bajo AM, Schally AV, Krupa M, Hebert F, Groot K, Szepeshazi K (2002) Bombesin antagonists inhibit growth of MDA-MB-435 estrogen-independent breast cancers and decrease the expression of the ErbB-2/HER-2 oncoprotein and c-jun and c-fos oncogenes. Proc Natl Acad Sci U S A 99, 3836-3841
7. Battey J, Wada E (1991) Two distinct receptor subtypes for mammalian bombesin-like peptides. Trends Neurosci 14, 524-8.
8. Benya RV, Fathi Z, Kusui T, Pradhan T, Battey JF, Jensen RT (1994) Gastrin-releasing peptide receptor-induced internalization, down-regulation, desensitization, and growth: possible role for cyclic AMP. Mol Pharmacol 46, 235-45.
9. Benya RV, Kusui T, Battey JF, Jensen RT (1995) Chronic desensitization and down-regulation of the gastrin-releasing peptide receptor are mediated by a protein kinase C-dependent mechanism. J Biol Chem 270, 3346-52.
10. Bocker D, Verspohl EJ (2001) Role of protein kinase C, PI3-kinase and tyrosine kinase in activation of MAP kinase by glucose and agonists of G-protein coupled receptors in INS-1 cells. Int J Exp Diabetes Res 2, 233-44.
11. Bold RJ, Kim HJ, Ishizuka J, Townsend CM Jr, Thompson JC (1998) A human gastric cancer cell line possesses a functional receptor for gastrin-releasing peptide. Cancer Invest 16, 12-7.
12. Bold RJ, Lowry PS, Ishizuka J, Battey JF, Townsend CM Jr, Thompson JC (1994) Bombesin stimulates the in vitro growth of a human gastric cancer cell line. J Cell Physiol 161, 519-25.
13. Bos JL, Franke B, M'Rabet L, Reedquist K, Zwartkruis F (1997) In search of a function for the Ras-like GTPase Rap1. FEBS Lett 410, 59-62.
14. Brown KD, Blakeley DM, Hamon MH, Laurie S, Corps AN (1987) Protein kinase C-mediated negative-feedback inhibition of unstimulated and bombesin-stimulated polyphosphoinositide hydrolysis in Swiss-mouse 3T3 cells. Biochem J 245, 631-9.
15. Burghardt B, Wenger C, Barabás K, Rácz G, Oláh A, Flautner L, Coy DH, Gress TM, Varga G (2001) GRPReceptor-mediated signal transduction, gene expression and DNA synthesis in the human pancreatic adenocarcinoma cell line HPAF. Peptides 22, 1119-28.
16. Chan AS, Wong YH (2004) Gbetagamma signaling and Ca2+ mobilization co-operate synergistically in a Sos and Rac-dependent manner in the activation of JNK by Gq-coupled receptors. Cell Signal 16, 823-36.
17. Chan AS, Wong YH (2005) Gq-mediated activation of c-Jun N-terminal kinase by the gastrin-releasing peptide-preferring bombesin receptor is inhibited upon costimulation of the Gs-coupled dopamine D1 receptor in COS-7 cells. Mol Pharmacol 68, 1354-64.
18. Charlesworth A, Rozengurt E (1997) Bombesin and neuromedin B stimulate the activation of p42(mapk) and p74(raf-1) via a protein kinase C-independent pathway in Rat-1 cells. Oncogene 14, 2323-9.
19. Chatzistamou I, Schally AV, Szepeshazi K, Groot K, Hebert F, Arencibia JM (2001) Inhibition of growth of ES-2 human ovarian cancers by bombesin antagonist RC-3095, and luteinizing hormone-releasing hormone antagonist Cetrorelix. Cancer Lett 171, 37-45.
20. Chinnappan D, Qu X, Xiao D, Ratnasari A, Weber HC (2008) Human gastrin-releasing peptide receptor gene regulation requires transcription factor binding at two distinct CRE sites. Am J Physiol Gastrointest Liver Physiol 295, G153-62.
21. Chu KU, Higashide S, Evers BM, Ishizuka J, Townsend CM Jr, Thompson JC (1995) Bombesin stimulates mucosal growth in jejunal and ileal Thiry-Vella fistulas. Ann Surg 221, 602-9.
22. Cornelio DB, Dal-Pizzol F, Roesler R, Schwartsmann G (2007) Targeting the bombesin/gastrin-releasing peptide receptor to treat sepsis. Recent Patents Anti-Infect Drug Disc 2, 178-81.
23. Cornelio D, Roesler R, Schwartsmann G (2007) Gastrin-releasing peptide receptor as a molecular target in experimental anticancer therapy. Ann. Oncol 18, 1457-66.
24. Corral RS, Iñiguez MA, Duque J, López-Pérez R, Fresno M (2007) Bombesin induces cyclooxygenase-2 expression through the activation of the nuclear factor of activated T cells and enhances cell migration in Caco-2 colon carcinoma cells. Oncogene 26, 958-69.
25. Dal-Pizzol F, Di Leone LP, Ritter C, Martins MR, Reinke A, Pens Gelain D, Zanotto-Filho A, de Souza LF, Andrades M, Barbeiro DF, Bernard EA, Cammarota M, Bevilaqua LR, Soriano FG, Cláudio J, Moreira F, Roesler R, Schwartsmann G (2006) Gastrin-releasing peptide receptor antagonist effects on an animal model of sepsis. Am J Respir Crit Care Med 173, 84-90.
26. de Oliveira MS, Cechim G, Braganhol E, Santos DG, Meurer L, de Castro CG Jr, Brunetto AL, Schwarstmann G, Battastini AM, Lenz G, Roesler R (2009) Anti-proliferative effect of the gastrin-release peptide receptor antagonist RC-3095 plus temozolomide in experimental glioblastoma models. J Neurooncol 93, 191-201.
27. Desai SJ, Ma AH, Tepper CG, Chen HW, Kung HJ (2006) Inappropriate activation of the androgen receptor by nonsteroids: involvement of the Src kinase pathway and its therapeutic implications. Cancer Res 66, 10449-59.
28. Donohue PJ, Sainz E, Akeson M, Kroog GS, Mantey SA, Battey JF, Jensen RT, Northup JK (1999) An aspartate residue at the extracellular boundary of TMII and an arginine residue in TMVII of the gastrin-releasing peptide receptor interact to facilitate heterotrimeric G protein coupling. Biochemistry 38, 9366-72.
29. Dorsam RT, Gutkind JS (2007) G-protein-coupled receptors and cancer. Nat Rev Cancer 7, 79-94.
30. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420, 629-35.
31. Fang MZ, Liu C, Song Y, Yang GY, Nie Y, Liao J, Zhao X, Shimada Y, Wang LD, Yang CS (2004) Over-expression of gastrin-releasing peptide in human esophageal squamous cell carcinomas. Carcinogenesis 25, 865-71.
32. Farias CB, Lima RC, Lima LO, Flores DG, Meurer L, Brunetto AL, Schwartsmann G, Roesler R (2008) Stimulation of proliferation of U138-MG glioblastoma cells by gastrin-releasing peptide in combination with agents that enhance cAMP signaling. Oncology 75, 27-31.
33. Farias CB, Stertz L, Lima RC, Kapczinski F, Schwartsmann G, Roesler R (2009) Reduced NGF secretion by HT-29 human colon cancer cells treated with a GRPR antagonist. Protein Pept Lett 16, 650-2.
34. Finn RS (2008) Targeting Src in breast cancer. Ann Oncol 19, 1379-86.
35. Fleischmann A, Waser B, Reubi JC (2007) Overexpression of gastrin-releasing peptide receptors in tumor-associated blood vessels of human ovarian neoplasms. Cell Oncol 29, 421-33.
36. Flores DG, de Farias CB, Leites J, de Oliveira MS, Lima RC, Tamajusuku AS, Di Leone LP, Meurer L, Brunetto AL, Schwartsmann G, Lenz G, Roesler R (2008) Gastrin-releasing peptide receptors regulate proliferation of C6 glioma cells through a phosphatidylinositol 3-kinase-dependent mechanism. Curr Neurovasc Res 5, 99-105.
37. Florin-Christensen J, Florin-Christensen M, Meinardi E, Calle R (1996) Diversity of roles of protein kinase C alpha in the proliferation of Swiss 3T3 cells. Biochem J 315 (Pt 2), 513-6.
38. Frankel A, Viallet J (1993) Protein kinase C is not involved in the homologous desensitization of bombesin responses in small cell lung cancer cells. Exp. Cell Res 209, 398-401.
39. Garcia LJ, Pradhan TK, Weber HC, Moody TW, Jensen RT (1997) The gastrin-releasing peptide receptor is differentially coupled to adenylate cyclase and phospholipase C in different tissues. Biochim Biophys Acta 1356, 343-54.
40. Gonzalez N, Moody TW, Igarashi H, Ito T, Jensen RT (2008) Bombesin-related peptides and their receptors: recent advances in their role in physiology and disease states. Curr Opin Endocrinol Diabetes Obes 1, 58-64.
41. Guo YS, Hellmich MR, Wen XD, Townsend CM Jr (2001) Activator protein-1 transcription factor mediates bombesin-stimulated cyclooxygenase-2 expression in intestinal epithelial cells. J Biol Chem 276, 22941-7.
42. Hellmich MR, Battey JF, Northup JK (1997) Selective reconstitution of gastrin-releasing peptide receptor with G alpha q. Proc Natl Acad Sci U S A 94, 751-6.
43. Hellmich MR, Ives KL, Udupi V, Soloff MS, Greeley GH Jr, Christensen BB, Townsend CM Jr (1999) Multiple protein kinase pathways are involved in gastrin-releasing peptide receptor-regulated secretion. J Biol Chem 274, 23901.
44. Heuser M, Schlott T, Schally AV, Kahler E, Schliephake R, Laabs SO, Hemmerlein B (2005) Expression of gastrin releasing Peptide receptor in renal cell carcinomas: a potential function for the regulation of neoangiogenesis and microvascular perfusion. J Urol 173, 2154-9.
45. Hohla F, Schally AV, Kanashiro CA, Buchholz S, Baker B, Kannadka C, Moder A, Aigner E, Datz C, Halmos G (2007) Growth inhibition of non-small-cell lung carcinoma by BB/GRP antagonist is linked with suppression of K-Ras, COX-2, and pAkt. Proc Natl Acad Sci U S A 104, 18671-6.
46. Hoosein NM, Logothetis CJ, Chung LW (1993) Differential effects of peptide hormones bombesin, vasoactive intestinal polypeptide and somatostatin analog RC-160 on the invasive capacity of human prostatic carcinoma cells. J Urol 149, 1209-13.
47. Iishi H, Tatsuta M, Baba M, Yamamoto R, Taniguchi H (1992) Enhancement by bombesin of colon carcinogenesis and metastasis induced by azoxymethane in Wistar rats. Int J Cancer 50, 834-9.
48. Ishola TA, Kang J, Qiao J, Evers BM, Chung DH (2007) Phosphatidylinositol 3-kinase regulation of gastrin-releasing peptide-induced cell cycle progression in neuroblastoma cells. Biochim Biophys Acta 1770, 927-32.
49. Jacamo R, Sinnett-Smith J, Rey O, Waldron RT, Rozengurt E (2008) Sequential Protein Kinase C (PKC)-dependent and PKC-independent Protein Kinase D Catalytic Activation via Gq-coupled Receptors: differential regulation of activation loop ser744 and ser748 phosphorylation. J Biol Chem 283, 12877-87.
50. Jensen RT, Battey JF, Spindel ER, Benya RV (2008) International Union of Pharmacology. LXVIII. Mammalian bombesin receptors: nomenclature, distribution, pharmacology, signaling, and functions in normal and disease states. Pharmacol Rev 60, 1-42.
51. Jia S, Roberts TM, Zhao JJ (2009) Should individual PI3 kinase isoforms be targeted in cancer? Curr Opin Cell Biol, in press.
52. Jian X, Sainz E, Clark WA, Jensen RT, Battey JF, Northup JK (1999) The bombesin receptor subtypes have distinct G protein specificities. J Biol Chem 274, 11573-81.
53. Kanashiro CA, Schally AV, Cai RZ, Halmos G (2005) Antagonists of bombesin/gastrin-releasing peptide decrease the expression of angiogenic and anti-apoptotic factors in human glioblastoma. Anticancer Drugs 16, 159-65.
54. Kanashiro CA, Schally AV, Zarandi M, Hammann BD, Varga JL (2007) Alterations of EGFR/HER, angiogenesis and apoptosis pathways after therapy with antagonists of growth hormone releasing hormone and bombesin in non-small cell lung cancer. Int J Oncol 30, 1019-28.
55. Kanashiro CA, Schally AV, Zarandi M, Hammann BD, Varga JL (2004) Suppression of growth of H-69 small cell lung carcinoma by antagonists of growth hormone releasing hormone and bombesin is associated with an inhibition of protein kinase C signaling. Int J Cancer 112, 570-6.
56. Kang J, Ishola TA, Baregamian N, Mourot JM, Rychahou PG, Evers BM, Chung DH (2007) Bombesin induces angiogenesis and neuroblastoma growth. Cancer Lett 253, 273-81.
57. Karlsson S, Ahrén B (1996) Gastrin-releasing peptide mobilizes calcium from intracellular stores in HIT-T15 cells. Peptides 17, 909-16.
58. Kiaris H, Schally AV, Sun B, Armatis P, Groot K (1999) Inhibition of growth of human malignant glioblastoma in nude mice by antagonists of bombesin/gastrin-releasing peptide. Oncogene 18, 7168-73.
59. Kim HJ, Evers BM, Litvak DA, Hellmich MR, Townsend CM Jr (2000) Signaling mechanisms regulating bombesin-mediated AP-1 gene induction in the human gastric cancer SIIA. Am J Physiol Cell Physiol 279, C326-34.
60. Kim S, Hu W, Kelly DR, Hellmich MR, Evers BM, Chung DH (2002) Gastrin-releasing peptide is a growth factor for human neuroblastomas. Ann Surg 235, 621-9.
61. Kroog GS, Sainz E, Worland PJ, Akeson MA, Benya RV, Jensen RT, Battey JF (1995) The gastrin-releasing peptide receptor is rapidly phosphorylated by a kinase other than protein kinase C after exposure to agonist. J Biol Chem 270, 8217-24.
62. Lacoste J, Aprikian AG, Chevalier S (2005) Focal adhesion kinase is required for bombesin-induced prostate cancer cell motility. Mol Cell Endocrinol 235, 51-61.
63. Levine L, Lucci JA, Pazdrak B, Cheng JZ, Guo YS, Townsend CM Jr, Hellmich MR (2003) Bombesin stimulates nuclear factor kappa B activation and expression of proangiogenic factors in prostate cancer cells. Cancer Res 63, 3495-502.
64. Li J, Hellmich MR, Greeley GH Jr, Townsend CM Jr, Evers BM (2002) Phorbol ester-mediated neurotensin secretion is dependent on the PKC-alpha and -delta isoforms. Am J Physiol Gastrointest Liver Physiol 283, G1197-206.
65. Lin X, Volkoff H, Narnaware Y, Bernier NJ, Peyon P, Peter RE (2000) Brain regulation of feeding behavior and food intake in fish. Comp Biochem Physiol A Mol Integr Physiol 126, 415-34.
66. Lin Y, Jian X, Lin Z, Kroog GS, Mantey S, Jensen RT, Battey J, Northup J (2000) Two amino acids in the sixth transmembrane segment of the mouse gastrin-releasing peptide receptor are important for receptor activation. J Pharmacol Exp Ther 294, 1053-62.
67. Liu X, Carlisle DL, Swick MC, Gaither-Davis A, Grandis JR, Siegfried JM (2007) Gastrin-releasing peptide activates Akt through the epidermal growth factor receptor pathway and abrogates the effect of gefitinib. Exp Cell Res 313, 1361-72.
68. Lui VW, Thomas SM, Zhang Q, Wentzel AL, Siegfried JM, Li JY, Grandis JR (2003) Mitogenic effects of gastrin-releasing peptide in head and neck squamous cancer cells are mediated by activation of the epidermal growth factor receptor. Oncogene 22, 6183-93.
69. Madarame J, Higashiyama S, Kiyota H, Madachi A, Toki F, Shimomura T, Tani N, Oishi Y, Matsuura N (2003) Transactivation of epidermal growth factor receptor after heparin-binding epidermal growth factor-like growth factor shedding in the migration of prostate cancer cells promoted by bombesin. Prostate 57, 187-95.
70. Manning BD (2004) Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J Cell Biol 167, 399-403.
71. McDonald TJ, Jörnvall H, Nilsson G, Vagne M, Ghatei M, Bloom SR, Mutt V (1979) Characterization of a gastrin releasing peptide from porcine non-antral gastric tissue. Biochem Biophys Res Commun 90, 227-33.
72. McDonald TJ, Nilsson G, Vagne M, Ghatei M, Bloom SR, Mutt V (1978) A gastrin releasing peptide from the porcine nonantral gastric tissue. Gut 19, 767-74.
73. Mitchell FM, Heasley LE, Qian NX, Zamarripa J, Johnson GL (1995) Differential modulation of bombesin-stimulated phospholipase C beta and mitogen-activated protein kinase activity by [D-Arg1,D-Phe5,D-Trp7,9,Leu11]substance P. J Biol Chem 270, 8623-8.
74. Nagakawa O, Ogasawara M, Murata J, Fuse H, Saiki I (2001) Effect of prostatic neuropeptides on migration of prostate cancer cell lines. Int J Urol 8, 65-70.
75. Ohki-Hamazaki H, Iwabuchi M, Maekawa F (2005) Development and function of bombesin-like peptides and their receptors. Int J Dev Biol 49, 293-300.
76. Oliveira PG, Brenol CV, Edelweiss MI, Brenol JC, Petronilho F, Roesler R, Dal-Pizzol F, Schwartsmann G, Xavier RM (2008) Effects of an antagonist of the bombesin/gastrin-releasing peptide receptor on complete Freund's adjuvant-induced arthritis in rats. Peptides 29, 1726-31.
77. Pang L, Decker SJ, Saltiel AR (1993) Bombesin and epidermal growth factor stimulate the mitogen-activated protein kinase through different pathways in Swiss 3T3 cells. Biochem J 289 (Pt1), 283-7.
78. Patel O, Dumesny C, Giraud AS, Baldwin GS, Shulkes A (2004) Stimulation of proliferation and migration of a colorectal cancer cell line by amidated and glycine-extended gastrin-releasing peptide via the same receptor. Biochem Pharmacol 68, 2129-42.
79. Patel O, Shulkes A, Baldwin GS (2006) Gastrin-releasing peptide and cancer. Biochim Biophys Acta 1766, 23-41.
80. Piiper A, Stryjek-Kaminska D, Klengel R, Zeuzem S (1997) CCK, carbachol, and bombesin activate distinct PLC-beta isoenzymes via Gq/11 in rat pancreatic acinar membranes. Am J Physiol 272(1 Pt 1), G135-40.
81. Pinski J, Schally AV, Halmos G, Szepeshazi K, Groot K (1994) Somatostatin analogues and bombesin/gastrin-releasing peptide antagonist RC-3095 inhibit the growth of human glioblastomas in vitro and in vivo. Cancer Res 54, 5895-901.
82. Plonowski A, Nagy A, Schally AV, Sun B, Groot K, Halmos G (2000) In vivo inhibition of PC-3 human androgen-independent prostate cancer by a targeted cytotoxic bombesin analogue, AN-215. Int J Cancer 88, 652-7.
83. Posern G, Weber CK, Rapp UR, Feller SM (1998) Activity of Rap1 is regulated by bombesin, cell adhesion, and cell density in NIH3T3 fibroblasts. J Biol Chem 273, 24297-300.
84. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, Ullrich A (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-8.
85. Qiao J, Kang J, Cree J, Evers BM, Chung DH (2005) Gastrin-releasing peptide-induced down-regulation of tumor suppressor protein PTEN (phosphatase and tensin homolog deleted on chromosome ten) in neuroblastomas. Ann Surg 241, 684-91.
86. Qiao J, Kang J, Ko TC, Evers BM, Chung DH (2006) Inhibition of transforming growth factor-beta/Smad signaling by phosphatidylinositol 3-kinase pathway. Cancer Lett 242, 207-14.
87. Qin Y, Ertl T, Cai RZ, Horvath JE, Groot K, Schally AV (1995) Antagonists of bombesin/gastrin-releasing peptide inhibit growth of SW-1990 human pancreatic adenocarcinoma and production of cyclic AMP. Int J Cancer 63, 257-62.
88. Radulovic S, Cai RZ, Serfozo P, Groot K, Redding TW, Pinski J, Schally AV (1991) Biological effects and receptor binding affinities of new pseudononapeptide bombesin/GRP receptor antagonists with N-terminal D-Trp or D-Tpi. Int J Pept Protein Res 38, 593-600.
89. Rey O, Sinnett-Smith J, Zhukova E, Rozengurt E (2001a) Regulated nucleocytoplasmic transport of protein kinase D in response to G protein-coupled receptor activation. J Biol Chem 276, 49228-35.
90. Rey O, Young SH, Cantrell D, Rozengurt E (2001b) Rapid protein kinase D translocation in response to G protein-coupled receptor activation: dependence on protein kinase C. J Biol Chem 276, 32616-26.
91. Rodríguez-Fernández JL, Rozengurt E (1998) Bombesin, vasopressin, lysophosphatidic acid, and sphingosylphosphorylcholine induce focal adhesion kinase activation in intact Swiss 3T3 cells. J Biol Chem 273, 19321-8.
92. Roelle S, Grosse R, Buech T, Chubanov V, Gudermann T (2008) Essential role of Pyk2 and Src kinase activation in neuropeptide-induced proliferation of small cell lung cancer cells. Oncogene 27, 1737-48.
93. Roesler R, Henriques JA, Schwartsmann G (2006a) Gastrin-releasing peptide receptor as a molecular target for psychiatric and neurological disorders. CNS Neurol Disord Drug Targets 5, 197-204.
94. Roesler R, Luft T, Oliveira SH, Farias CB, Almeida VR, Quevedo J, Dal Pizzol F, Schröder N, Izquierdo I, Schwartsmann G (2006b) Molecular mechanisms mediating gastrin-releasing peptide receptor modulation of memory consolidation in the hippocampus. Neuropharmacology 51, 350-7.
95. Rozengurt E (2007) Mitogenic signaling pathways induced by G protein-coupled receptors. J Cell Physiol 213, 589-602.
96. Rozengurt E (1998) Signal transduction pathways in the mitogenic response to G protein-oupled neuropeptide receptor agonists. J Cell Physiol 177, 507-17.
97. Rozengurt E, Guha S, Sinnett-Smith J (2002) Gastrointestinal peptide signalling in health and disease. Eur J Surg Suppl 587, 23-38.
98. Rozengurt E, Rey O, Waldron RT (2005) Protein kinase D signaling. J Biol Chem 280, 13205-8.
99. Rozengurt E, Sinnett-Smith J (1983) Bombesin stimulation of DNA synthesis and cell division in cultures of Swiss 3T3 cells. Proc Natl Acad Sci U S A 80, 2936-40.
100. Sahai E, Marshall CJ (2002) RHO-GTPases and cancer. Nat Rev Cancer 2, 133-42.
101. Sakamoto H, Matsuda K, Zuloaga DG, Hongu H, Wada E, Wada K, Jordan CL, Breedlove SM, Kawata M (2008) Sexually dimorphic gastrin releasing peptide system in the spinal cord controls male reproductive functions. Nat Neurosci 11, 634-6.
102. Salazar EP, Hunger-Glaser I, Rozengurt E (2003) Dissociation of focal adhesion kinase and paxillin tyrosine phosphorylation induced by bombesin and lysophosphatidic acid from epidermal growth factor receptor transactivation in Swiss 3T3 cells. J Cell Physiol 194, 314-24.
103. Salmena L, Carracedo A, Pandolfi PP (2008) Tenets of PTEN tumor suppression. Cell 133, 403-14.
104. Santiskulvong C, Rozengurt E (2007) Protein kinase Calpha mediates feedback inhibition of EGF receptor transactivation induced by Gq-coupled receptor agonists. Cell Signal 19, 1348-57.
105. Santiskulvong C, Sinnett-Smith J, Rozengurt E (2004) Insulin reduces the requirement for EGFR transactivation in bombesin-induced DNA synthesis. Biochem Biophys Res Commun 318, 826-32.
106. Saurin JC, Fallavier M, Sordat B, Gevrey JC, Chayvialle JA, Abello J (2002) Bombesin stimulates invasion and migration of Isreco1 colon carcinoma cells in a Rho-dependent manner. Cancer Res 62, 4829-35.
107. Schwartsmann G, DiLeone LP, Horowitz M, Schunemann D, Cancella A, Pereira AS, Richter M, Souza F, da Rocha AB, Souza FH, Pohlmann P, De Nucci G (2006) A phase I trial of the bombesin/gastrin-releasing peptide (BB/GRP) antagonist RC3095 in patients with advanced solid malignancies. Invest New Drugs 24, 403-12.
108. Seensalu R, Avedian D, Barbuti R, Song M, Slice L, Walsh JH (1997) Bombesin-induced gastrin release from canine G cells is stimulated by Ca2+ but not by protein kinase C, and is enhanced by disruption of rho/ cytoskeletal pathways. J Clin Invest 100, 1037-46.
109. Seethala RR, Gooding WE, Handler PN, Collins B, Zhang Q, Siegfried JM, Grandis JR (2008) Immunohistochemical analysis of phosphotyrosine signal transducer and activator of transcription 3 and epidermal growth factor receptor autocrine signaling pathways in head and neck cancers and metastatic lymph nodes. Clin Cancer Res 14, 1303-9.
110. Seufferlein T, Withers DJ, Mann D, Rozengurt E (1996) Dissociation of mitogen-activated protein kinase activation from p125 focal adhesion kinase tyrosine hosphorylation in Swiss 3T3 cells stimulated by bombesin, lysophosphatidic acid, and platelet-derived growth factor. Mol Biol Cell 7, 1865-75.
111. Shapira H, Amit I, Revach M, Oron Y, Battey JF (1998) Galpha14 and Galphaq mediate the response to trypsin in Xenopus oocytes. J Biol Chem 273, 19431-6.
112. Sharif TR, Luo W, Sharif M (1997) Functional expression of bombesin receptor in most adult and pediatric human glioblastoma cell lines; role in mitogenesis and in stimulating the mitogen-activated protein kinase pathway. Mol Cell Endocrinol 130, 119-30.
113. Sinnett-Smith J, Jacamo R, Kui R, Wang YM, Young SH, Rey O, Waldron RT, Rozengurt E (2009) Protein kinase D mediates mitogenic signaling by Gq-coupled receptors through PKC-independent regulation of activation loop Ser744 and Ser748 phosphorylation. J Biol Chem 284, 13434-45.
114. Sinnett-Smith J, Santiskulvong C, Duque J, Rozengurt E (2000) [D-Arg(1),D-Trp(5,7,9),Leu(11)]Substance P inhibits bombesin-induced mitogenic signal transduction mediated by both G(q) and G(12) in Swiss 3T3cells. J Biol Chem 275, 30644-52.
115. Sinnett-Smith J, Zhukova E, Rey O, Rozengurt E (2007) Protein kinase D2 potentiates MEK/ERK/RSK signaling, c-Fos accumulation and DNA synthesis induced by bombesin in Swiss 3T3 cells. J Cell Physiol 211, 781-90.
116. Stangelberger A, Schally AV, Varga JL, Zarandi M, Cai RZ, Baker B, Hammann BD, Armatis P, Kanashiro CA (2005) Inhibition of human androgen-independent PC-3 and DU-145 prostate cancers by antagonists of bombesin and growth hormone releasing hormone is linked to PKC, MAPK and c-jun intracellular signalling. Eur J Cancer 41, 2735-44.
117. Steinberg SF (2008) Structural basis of protein kinase C isoform function. Physiol Rev 88, 1341-78.
118. Swope SL, Schonbrunn A (1990) Desensitization of islet cells to bombesin involves both receptor down- modulation and inhibition of receptor function. Mol Pharmacol 37, 758-66.
119. Szepeshazi K, Schally AV, Halmos G, Lamharzi N, Groot K, Horvath JE (1997) A single in vivo administration of bombesin antagonist RC-3095 reduces the levels and mRNA expression of epidermal growth factor receptors in MXT mouse mammary cancers. Proc Natl Acad Sci U S A 94, 10913-8.
120. Taglia L, Matusiak D, Matkowskyj KA, Benya RV (2007) Gastrin-releasing peptide mediates its morphogenic properties in human colon cancer by upregulating intracellular adhesion protein-1 (ICAM-1) via focal adhesion kinase. Am J Physiol Gastrointest Liver Physiol 292, G182-90.
121. Takahashi A, Tanaka S, Miwa Y, Yoshida H, Ikegami A, Niikawa J, Mitamura K (2000) Involvement of calmodulin and protein kinase C in cholecystokinin release by bombesin from STC-1 cells. Pancreas 21, 231-9.
122. Takemura H, Ohshika H (1999) Capacitative Ca2+ entry involves Ca2+ influx factor in rat glioma C6 cells. Life Sci 64, 1493-500.
123. Thomas SM, Grandis JR, Wentzel AL, Gooding WE, Lui VW, Siegfried JM (2005) Gastrin-releasing peptide receptor mediates activation of the epidermal growth factor receptor in lung cancer cells. Neoplasia 7, 426-31.
124. Tsuda T, Kusui T, Hou W, Benya RV, Akeson MA, Kroog GS, Battey JF, Jensen RT (1997) Effect of gastrin-releasing peptide receptor number on receptor affinity, coupling, degradation, and modulation. Mol Pharmacol 51, 721-32.
125. Vivanco I, Sawyers CL (2002) The phosphatidylinositol 3-kinase-akt pathway in human cancer. Nat Rev Cancer 2, 489-501.
126. Walsh JH, Bouzyk M, Rozengurt E (1993) Homologous desensitization of bombesin-induced increases in intracellular Ca2+ in quiescent Swiss 3T3 cells involves a protein kinase C-independent mechanism. J Cell Physiol 156, 333-340.
127. Wang LH, Battey JF, Wada E, Lin JT, Mantey S, Coy DH, Jensen RT (1992) Activation of neuromedin B-preferring bombesin receptors on rat glioblastoma C-6 cells increases cellular Ca2+ and phosphoinositides. Biochem J 286 (Pt 2), 641-8.
128. Wang QJ (2006) PKD at the crossroads of DAG and PKC signaling. Trends Pharmacol Sci 27, 317-23.
129. Wang SI, Puc J, Li J, Bruce JN, Cairns P, Sidransky D, Parsons R (1997) Somatic mutations of PTEN in glioblastoma multiforme. Cancer Res 57, 4183-6.
130. Weber HC (2009) Regulation and signaling of human bombesin receptors and their biological effects. Curr Opin Endocrinol Diabetes Obes 16, 66-71.
131. Weber HC, Jensen RT, Battey JF (2000) Molecular organization of the mouse gastrin-releasing peptide receptor gene and its promoter. Gene 244, 137-49.
132. Weber S, Zuckerman JE, Bostwick DG, Bensch KG, Sikic BI, Raffin TA (1985) Gastrin releasing peptide is a selective mitogen for small cell lung carcinoma in vitro. J Clin Invest 75, 306-9.
133. Wong ST, Athos J, Figueroa XA, Pineda VV, Schaefer ML, Chavkin CC, Muglia LJ, Storm DR (1999) Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23, 787-98.
134. Wu B, Wang H, Qing WJ (2007) Bombesin increases cytokeratin expression and free calcium concentration in PC-3 cell line. Zhonghua Nan Ke Xue 13, 332-4.
135. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124, 471-84.
136. Xiao D, Qu X, Weber HC (2003) Activation of extracellular signal-regulated kinase mediates bombesin-induced mitogenic responses in prostate cancer cells. Cell Signal 15, 945-53.
137. Yan Y, Shirakabe K, Werb Z (2002) The metalloprotease Kuzbanian (ADAM10) mediates the transactivation of EGF receptor by G protein-coupled receptors. J Cell Biol 158, 221-6.
138. Yuan J, Rey O, Rozengurt E (2006) Activation of protein kinase D3 by signaling through Rac and the alpha subunits of the heterotrimeric G proteins G12 and G13. Cell Signal 18, 1051-62.
139. Yuan J, Slice L.W.; Rozengurt E (2001) Activation of protein kinase D by signaling through Rho and the alpha subunit of the heterotrimeric G protein G13. J Biol Chem 276, 38619-27.
140. Zachary I, Sinnett-Smith J, Turner C, Rozengurt E (1993) Bombesin, vasopressin, and endothelin rapidly stimulate tyrosine phosphorylation of the focal adhesion-associated protein paxillin in Swiss 3T3 cells. J Biol Chem 268, 22060-5.
141. Zhang H, Liu G, Dziubinski M, Yang Z, Ethier SP, Wu G (2008) Comprehensive analysis of oncogenic effects of PIK3CA mutations in human mammary epithelial cells. Breast Cancer Res Treat 112, 217-27.
142. Zhang Q, Bhola NE, Lui VW, Siwak DR, Thomas SM, Gubish CT, Siegfried JM, Mills GB, Shin D, Grandis JR (2007) Antitumor mechanisms of combined gastrin-releasing peptide receptor and epidermal growth factor receptor targeting in head and neck cancer. Mol Cancer Ther 6, 1414-24.
143. Zhang Q, Thomas SM, Lui VW, Xi S, Siegfried JM, Fan H, Smithgall TE, Mills GB, Grandis JR (2006) Phosphorylation of TNF-alpha converting enzyme by gastrin-releasing peptide induces amphiregulin release and EGF receptor activation. Proc Natl Acad Sci U S A 103, 6901-6.
144. Zhang Q, Thomas SM, Xi S, Smithgall TE, Siegfried JM, Kamens J, Gooding WE, Grandis JR (2004) SRC family kinases mediate epidermal growth factor receptor ligand cleavage, proliferation, and invasion of head and neck cancer cells. Cancer Res 64, 6166-73.
145. Zheng R, Iwase A, Shen R, Goodman OB Jr, Sugimoto N, Takuwa Y, Lerner DJ, Nanus DM (2006) Neuropeptide-stimulated cell migration in prostate cancer cells is mediated by RhoA kinase signaling and inhibited by neutral endopeptidase. Oncogene 25, 5942-52.
146. Zhou J, Chen J, Mokotoff M, Ball ED (2004) Targeting gastrin-releasing peptide receptors for cancer treatment. Anticancer Drugs 15, 921-7.
147. Zugaza JL, Waldron RT, Sinnett-Smith J, Rozengurt E (1997) Bombesin, vasopressin, endothelin, bradykinin, and platelet-derived growth factor rapidly activate protein kinase D through a protein kinase C-dependent signal transduction pathway. J Biol Chem 272, 23952-60.